Microsaccades mediate perceptual alternations in Monet's "Impression, sunrise" - Nature
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OPEN Microsaccades mediate perceptual
alternations in Monet’s
“Impression, sunrise”
Robert G. Alexander1, Ashwin Venkatakrishnan1, Jordi Chanovas1,2, Stephen L. Macknik1 &
Susana Martinez‑Conde1*
Troxler fading, the perceptual disappearance of stationary images upon sustained fixation, is
common for objects with equivalent luminance to that of the background. Previous work showed
that variations in microsaccadic rates underlie the perceptual vanishing and intensification of simple
stimuli, such as Gabor patches. Here, we demonstrate that microsaccade dynamics also contribute
to Troxler fading and intensification during the viewing of representational art. Participants fixated a
small spot while viewing either a Gabor patch on a blank background, or Monet’s painting “Impression,
Sunrise.” They continuously reported, via button press/release, whether the Gabor patch, or the sun
in Monet’s painting, was fading versus intensifying, while their eye movements were recorded with
high precision. Microsaccade rates peaked before reports of increased visibility, and dropped before
reports of decreased visibility or fading, both when viewing Gabor patches and Monet’s sun. These
results reveal that the relationship between microsaccade production and the reversal and prevention
of Troxler fading applies not only to the viewing of contrived stimuli, but also to the observation
of “Impression, Sunrise.” Whether or not perceptual fading was consciously intended by Monet,
our findings indicate that observers’ oculomotor dynamics are a contributor to the cornerstone of
Impressionism.
“Impression, Sunrise,” created by the French painter Claude Monet in 1872, is credited with inspiring the name
of the Impressionist movement. The painting depicts the harbor of Le Havre in France, as seen from Monet’s
window (Fig. 1A). This was not Monet’s actual view of the scene—as he explained—but his “impression,” hence
the title. Indeed, one way in which “Impression, Sunrise” departs from reality is that the rising sun appears sub-
stantially brighter than the adjacent sky. Whereas this is true in life (i.e. the sun’s luminance is actually greater
than that of the sky), the viewer’s perception of Monet’s sun as more brilliant than its surroundings is an illusion.
Grayscale renderings of “Impression, Sunrise” show that the sun has the same physical luminance as the back-
ground clouds. This equiluminant quality may be critical to the painting’s “eerie” lifelike appearance, in which
the sun “seems to pulsate” against the s ky1.
Over two decades ago, Safran and L andis2 noticed that staring for a few seconds at the head of the sailor
standing in the boat in Monet’s painting causes the sun to seemingly fade away. The perceptual result is a
sunless sky, as the region occupied by the vanished sun fills in with visual information from the surrounding
background. Safran and Landis suggested that such fading—and subsequent filling-in—of Monet’s sun is due
to the phenomenon known as Troxler fading. This hypothesis is supported by prior reports that Troxler fading,
the perceptual disappearance of stationary images upon sustained fixation, is quite common for peripheral
objects with equivalent luminance to that of the b ackground3–6. However, no previous studies have quantified
the temporal dynamics of perceptual fading in “Impression, Sunrise,” or determined their potential relationship
to ongoing fixational eye movements.
Here, we set out to determine if changes in the production of microsaccades—small, involuntary eye move-
ments occurring a few times a second during fixation—drive the perceptual disappearance (and eventual reap-
pearance) of the sun in Monet’s painting. Previous studies have shown that variations in microsaccadic rates
underlie the perceptual vanishing and intensification of simple, contrived visual stimuli (i.e., Gabor patches),
presented in the context of Troxler fading tasks7–11. Were a similar relationship between oculomotor and percep-
tual dynamics to be found for “Impression, Sunrise,” it would support the proposal that the illusory vanishing
1
Department of Ophthalmology, SUNY Downstate Health Sciences University, Brooklyn, NY, USA. 2Graduate
Program in Neural and Behavioral Science, SUNY Downstate Health Sciences University, Brooklyn, NY,
USA. *email: smart@neuralcorrelate.com
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of Monet’s sun constitutes an instantiation of Troxler fading in the art domain. In addition, it would indicate the
relevance of observers’ fixational eye movement dynamics to their experience of Monet’s masterpiece.
Methods
Participants. Twenty-two participants (12 males, 10 females; ages ranged from 15 to 54, with an average of
28.3 years), with normal or corrected-to-normal vision, participated in the experiment. Eighteen participants
were naïve and were paid $15/session. All experiments were performed in accordance with relevant guidelines
and regulations. Ethical clearance was approved by the SUNY Downstate Institutional Review Board (protocol
number 690152) and the experiments were performed in accordance with the Declaration of Helsinki. Written
informed consent was obtained from each participant. One additional participant was discarded, because their
“Gabor Condition” data (which served as control for the “Monet Condition,” see below) failed to produce the
known relationship between ocular events and perceptual fading d ynamics7,8,10 that serves as the basis for com-
parison with the “Monet Condition” data in the present study (as detailed below).
Experimental design. Participants rested their forehead and chin on the EyeLink 1000 head/chin sup-
port, ~ 72.0 cm away from a linearized video monitor (Barco Reference Calibrator V, 60 Hz refresh rate). The
experiment consisted of 252 pseudorandomly-interleaved 30-s trials. After 30 s, all stimuli disappeared and the
trial ended. To disregard the potential effect of the initial stimulus onset transient at the start of each trial, we
conducted analyses only on data recorded after both the first second of the trial and the first button press (which
indicated the first perceptual transition toward fading).
While fixating a small red spot (0.1° diameter), participants were asked to continuously report whether an
unchanging stimulus (the sun in the Monet Condition, and a Gabor patch in the Gabor Condition) was faded/
fading (button press) or intensified/intensifying (button release)7–10. The stimulus did not change physically, but
it appeared to fade or intensify as a function of the observer’s fixation dynamics—see Fig. 1B. Naïve participants
were not informed, before the experiment, that the only changes to the appearance of the stimulus would be
illusory.
The experiment included three kinds of trials. Here we present data from the Monet Condition and the Gabor
Condition only. The third type of trial consisted of images of an unrelated painting (72 trials total), which were
used in a different project and not discussed further here.
Monet condition. A reproduction of Monet’s “Impression, Sunrise” was presented on 36 trials, and a mir-
ror-image of the same painting (horizontally-flipped, to lessen the effect of contrast adaptation across trials) was
presented on another 36 interleaved trials. Thus, there were 72 “Monet” trials total, in which participants looked
at a fixation target (a red spot of 0.1° diameter, placed on the hat of the standing fisherman), and simultaneously
reported, at all times, whether the depicted sun was in the process of fading or intensifying (Fig. 1). The painting
was centered on the monitor, in both its original orientation and as a horizontally-flipped mirror-image. As a
result, the sun appeared on either the left or the right side of fixation. The painting’s digital reproduction used
here was directly acquired from the Muséeum Marmottan Monet (which holds the original painting in their
collection). This digital image had a resolution of 8241 × 6312, which we then down sampled to 1468 × 1125 to
achieve a distance of 9° from the fixation target to the center of the sun (for the purpose of data comparisons
between the Monet Condition and the Gabor Condition).
Gabor condition. The Gabor Condition served as a control condition against which to compare the results
from the Monet Condition. Thus, the Gabor trials were designed to reproduce the visual stimuli presented in
prior research showing a causal relationship between changes in microsaccade dynamics and perceptual alterna-
tions during Troxler fading7–11. Following from this, we presented a two-lobe Gabor patch with peak-to-trough
width of 2.5° (with axis parallel to the carrier grating). The Gaussian SDs were x = 1.5° and y = 1°, with a sinu-
soidal grating having a period of 5° and phase of 0. The Gabor had a maximum contrast of 40% from peak-to-
trough and the same average luminance (50%) as the background. The position of the Gabor varied randomly
across trials at one of eight points of the compass (0°, 45°, 90°, …, 315°) to control for possible contrast adapta-
tion effects across trials. The orientation of the Gabor also varied randomly between 0° and 360° (35 different ori-
entations varying in steps of 10° from 0° to 360°) in each trial to control for orientation adaptation effects. As on
Monet trials, the distance from the fixation target (a red spot of 0.1° diameter placed on the center of the screen)
to the center of the fading stimulus (i.e. the Gabor patch) was fixed at 9°. This condition included 108 trials.
Eye movement analysis. Eye position was acquired noninvasively with a fast video-based eye tracker at
500 Hz (EyeLink 1000, SR Research). We recorded eye movements simultaneously in both eyes, identifying and
removing blink periods as portions of the raw data where pupil information was missing. We also removed por-
tions of data where very fast decreases and increases in pupil area occurred (> 50 units per sample; such periods
might indicate semi-blinks where the pupil is never fully occluded)12,13. In addition, we removed 200 ms of raw
data before and after each blink/semi-blink to eliminate the initial and final parts where the pupil was still par-
tially occluded12. Saccades were identified with a modified version of the algorithm developed by Engbert and
Kliegl et al.14–18, with λ = 6 (used to obtain the velocity threshold) and a minimum saccadic duration of 6 ms. To
reduce the amount of potential noise, we considered only binocular saccades, that is, saccades with a minimum
overlap of one data sample in both e yes15–18. Moreover, we imposed a minimum intersaccadic interval of 20 ms
so that potential overshoot corrections might not be categorized as new saccades19. To calculate microsaccade
properties such as magnitude and peak velocity, we averaged the values for the right and left eyes. Figure 2 shows
the peak velocity-magnitude relationship (Fig. 2A,B) and the magnitude distribution (Fig. 2C,D) for (micro)
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Figure 1. Experimental design. (A) Monet’s “Impression, soleil levant,” presented at its original orientation,
with the addition of a red spot on the hat of the person standing in the boat. This red spot served as a fixation
target during the experiment. To experience the perceptual fading of the sun, look at the red spot and hold your
gaze still for about a minute while covertly focusing your attention on the sun. (B) Epochs from a Monet trial.
The physical stimulus is shown in the top row, the participant’s perception of the stimulus in the second row, and
the participant’s report in the third row. The perceptual experience is consistent with Troxler f ading1: the sun
disappears perceptually, and fills-in with the colour of the surrounding background. The fixation spot is not to
scale. Reproduction from Musee Marmottan Monet, Paris, France/Bridgeman Images.
saccades with magnitudes up to 2°). All subsequent analyses (Fig. 3) concern microsaccades only, that is, sac-
cades with magnitudes < 1°. (Saccadic magnitude thresholds of 1.5°, 2°, and 3° produced comparable results; see
Supplementary Fig. 1).
Microsaccade correlations with reported transitions. Let XM and XR be the stochastic processes rep-
resenting the onsets of microsaccade, and intensification report (R). For example, if S1, S2, …, Sk are the start
times of all the microsaccades for a given subject, then XM for that subject will be given by XM(t) = 1 if t = Si for
some 1 ≤ i ≤ k and XM(t) = 0 otherwise; similarly for intensification reports.
We obtained correlations of microsaccades with reports of intensification for each subject, using ξ MR(t)
m=−∞ X m(n + t)XR(n) and then converting it to a rate (similarly for transitions to fading) . For each
8
= n=∞
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Figure 2. Microsaccade characterization and perceptual reports. (A,B) Peak velocity-magnitude relationship
for all (micro)saccades with magnitudes < 2°. (C,D) Distribution of (micro)saccade magnitudes for the
participant average. (E,F) Distribution of intensifying (red) and fading (blue) periods during the Monet and
Gabor conditions, as indicated by the participants’ report. Shading indicates the SEM across participants. N = 22
participants for each plot.
participant, correlations were smoothed using a Savitsky–Golay filter of order 1 and a window size of 151 ms7.
Average correlations are the average of the smoothed correlations (Fig. 3).
Microsaccade correlation baselines. For each condition (e.g. Monet or Gabor), we defined the micro-
saccade rate baseline as the rate of microsaccades produced far from the changes in visibility that took place
during those trials. Thus, we calculated these microsaccadic rates using data 700 ms away from all reported
transitions (i.e. perceptual intensification or fading) in both directions of time. The microsaccades produced
during this period are independent of the perceptual transitions, as they occurred outside of subjects’ reaction
times window in both directions of time8,9.
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Figure 3. Microsaccade dynamics before transitions toward perceptual intensification versus fading. Average
probability of microsaccades before transitions toward perceptual intensification (red) versus fading (blue)
for (A) Monet’s sun and (B) a Gabor patch. The solid vertical line indicates the reported transitions (time = 0).
The grey dashes along the top of the plots indicate the bins where microsaccade rates before transitions to
intensification were significantly higher than microsaccade rates before transitions to fading (two-tailed paired
t tests with Bonferroni correction, bin size = 20 ms, p < 0.05). Red and blue shading indicates the SEM across
subjects (N = 22). Because trials from the two conditions were interleaved, both panels show data from the same
participants, collected during the same sessions.
Statistical methods. To test whether microsaccade rates before transitions to intensification were signifi-
cantly higher than those before transitions to fading, we performed two-tailed paired t-tests in each bin (bin
size = 20 ms), using Bonferroni correction to account for multiple comparisons (Fig. 3). All other statistical tests
were likewise two-tailed paired t-tests. Significance levels were set to α = 0.01 throughout.
Results
Participants fixated a small spot while viewing either a Gabor patch on a blank background, or Monet’s painting
“Impression, Sunrise” (Fig. 1A). They continuously reported, via button press/release, whether the Gabor patch,
or the sun in Monet’s painting, was fading versus intensifying. Their eye movements were recorded simultane-
ously with high precision (for details, see Materials and Methods). Figure 1B describes a typical epoch during
a trial.
As with other bistable stimuli p aradigms7,20–23, participants reported that their perception oscillated between
two alternating states (faded/fading vs. visible/intensifying), both for the Gabor p atch7–11 and for Monet’s sun1,
even though neither stimulus changed physically over the course of a trial.
Both the Gabor and the Monet sun stimuli faded for a substantial amount of time, without a significant
difference in percept duration (for either faded or visible percepts) between the Gabor and Monet conditions
(t(42) = − 1.91, p = 0.06, 95% CI [− 4.08, 0.11] for intensification; t(42) = − 0.19, p = 0.85, 95% CI [-1.05, 0.87] for
fading, see Fig. 2E,F).
Oculomotor behavior was also equivalent across the Gabor and the Monet conditions. For example, the
microsaccade main sequences (peak velocity-magnitude relationships) were comparable for both types of trials
(t(42) = 0.15, p = 0.88, 95% CI [− 4.83, 5.6], see Fig. 2A,B), and so were the microsaccade magnitude distribu-
tions, t(42) = − 0.42, p = 0.67, 95% CI [− 0.16, 0.1]; see Fig. 2C,D). See Table 1 for additional statistics regarding
the participants’ oculomotor dynamics and perceptual reports.
Next, we examined the timing of microsaccades with respect to that of perceptual alternations, by locking
changes in microsaccade rates to changes in perceptual transition reports. This analysis revealed a clear relation-
ship between microsaccade production and fading/intensification dynamics. Specifically, we found that increased
microsaccade rates were related to perceptual intensification/visibility. Conversely, decreased microsaccade rates
were related to perceptual fading (Fig. 3 and Supplementary Figs. 1 and 3). Importantly, the relationship between
microsaccade production and the perceptual intensification/fading of Monet’s sun mirrored such a relationship
in the case of the Gabor patch—which itself replicated previous findings connecting microsaccade production
to the reversal of Troxler fading7–11.
Our combined results provide the first quantification of eye movement dynamics as related to the perception
of visibility in a critical element of Monet’s masterpiece. They moreover suggest that the vibrant, pulsating quality
of Monet’s s un1 results from the viewer’s own oculomotor behavior.
Discussion
In this study, we show that changes in microsaccade production underlie the intermittent vanishing and reap-
pearance of the sun in Claude Monet’s “Impression, Sunrise,” thereby indicating that such perceptual alternations
are an instantiation of Troxler fading in this iconic masterpiece.
Prior work has linked Troxler fading to neural adaptation to unchanging stimuli24–26. Abrupt retinal motion
from microsaccades (and other transient oculomotor events, such as larger saccades and blinks) has been shown
to counteract such adaptation and consequently restore the visibility of previously faded visual o bjects7–11.
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Monet condition Gabor condition
Number of trials 72 108
Number of microsaccades 1399 ± 127 per subject (19.43 ± 1.76 per trial) 2165 ± 192 per subject (20.05 ± 1.78 per trial)
Microsaccade rate (N/s) 0.67 ± 0.06 0.69 ± 0.06
Microsaccade magnitude (°) 0.44 ± 0.02 0.47 ± 0.02
Microsaccade duration (ms) 14.33 ± 0.65 15.18 ± 0.69
Microsaccade peak velocity (°/s) 47.09 ± 1.89 49.37 ± 2.08
Number of transitions to fading (N) 215.27 ± 28.01 per subject (2.99 ± 0.35 per trial) 405.82 ± 39.28 per subject (3.76 ± 0.33 per trial)
Duration of perceived fading periods subsequent to the first 1 s of the trial (s) 6.95 ± 0.87 total per trial 8.32 ± 0.83 total per trial
Duration of first fading period after stimulus onset (s) 3.04 ± 0.61 2.76 ± 0.41
Time spent in fading periods
23.96 ± 3.00 28.67 ± 2.87
(% of trial)
Number of transitions to intensifying (N) 192.23 ± 26.96 per subject (2.67 ± 0.34 per trial) 368.54 ± 37.81 per subject (3.41 ± 0.35 per trial)
Duration of perceived intensifying periods subsequent to the first 1 s of the trial
9.12 ± 0.62 total per trial 11.27 ± 0.43 total per trial
(s)
Time spent in intensifying periods (% of trial) 31.44 ± 2.15 38.82 ± 1.47
Table 1. Average microsaccade and perceptual parameters. Number of microsaccades, microsaccade rate,
magnitude, duration, and peak velocity, were calculated for saccadic movements with a magnitude ≤ 1°.
However, no prior study had demonstrated the impact of this perceptual phenomenon in a viewer’s experience
of visual art, especially in connection to the observer’s own gaze behaviour. The effects of changing microsaccade
dynamics on Troxler fading have been previously shown with Gabor patches, well-controlled visual stimuli that
are frequently used in psychophysical experiments7–11. Here, we asked if microsaccade production had com-
parable effects on the visibility of both Gabor patches and the sun in Monet’s painting. Thus, our experimental
design included a number of Gabor trials, in which the stimuli characteristics precisely replicated those used
in our earlier r esearch8,10. Consequently, we were able to correlate microsaccades to perceptual reports for both
Gabor patches and Monet’s sun, and compare the results across the two types of trials.
Time-locked analyses of microsaccades and perceptual reports (button presses and releases) revealed several
key findings. First, in agreement with previous s tudies8–11, we found that microsaccade rates decreased before
reports of perceptual fading and increased before reports of perceptual intensification, showing that microsac-
cades both prevent and counteract the incidence of Troxler fading in Gabor patches. Second, we extended the
above findings to a more naturalistic context: the viewing of artwork. We demonstrated that the relationship
between microsaccade production and the reversal and prevention of Troxler fading applies not only to the
viewing of contrived stimuli such as Gabor patches, but also to the observation of Monet’s masterpiece. Oculo-
motor and perceptual dynamics, and the relationship between them, were quantitatively equivalent for Gabor
and Monet trials, including but not limited to the duration of fading and intensification periods, the slope of
the (micro)saccadic peak velocity-magnitude relationship, and the temporal correlations between microsaccade
onsets and perceptual reports of fading and intensification. We note that the relationship between microsaccade
dynamics and target visibility found here is also likely to apply to other transient oculomotor events (including
larger saccades and blinks), as previously reported for the perception of Gabor patches during Troxler f ading8,9,
as well as that of illusory motion from static repetitive p atterns27.
We might speculate as to whether Monet—intentionally or intuitively—controlled the composition so that
the sun faded when viewers sustained their gaze upon a specific focal point of the painting—such as the sailor.
It is widely accepted that artists emphasize and exploit the perceptual skills of observers through both creative
intuition and artistic skill28. Thus, Monet may have adjusted the visual qualities of his painting to produce a depic-
tion of the sun that is prone to fading (specifically, by minimizing the luminance contrast between the sun and
its immediate surroundings). In that case, Monet could have intended the perceptual fading of the sun, making
specific choices about the visual organization in “Impression, Sunrise” to influence the viewers’ experience of
the art. Alternatively, Monet may have chosen the properties of the depicted sun for other purposes, in a way
that coincidentally facilitates fading.
Whether or not perceptual fading was calculated by Monet, the qualities of depicted objects hold the potential
to alter viewers’ experience of the artwork. Our results support the proposal that Troxler fading drives the illusory
vanishing of the sun in Monet’s “Impression, Sunrise,” and suggest that observers’ oculomotor dynamics are a
meaningful contributor to their perception of this cornerstone of Impressionism.
Received: 17 April 2020; Accepted: 18 January 2021
References
1. Livingstone, M. S. Vision and Art: The Biology of Seeing (Abrams, New York, 2002).
2. Safran, A. B. & Landis, T. The vanishing of the sun: A manifestation of cortical plasticity. Surv. Ophthalmol. 42, 449–452 (1998).
3. De Weerd, P. Perceptual filling-in: More than the eye can see. Prog. Brain Res. 154, 227–245 (2006).
Scientific Reports | (2021) 11:3612 | https://doi.org/10.1038/s41598-021-82222-3 6
Vol:.(1234567890)www.nature.com/scientificreports/
4. Livingstone, M. S. & Hubel, D. H. Psychophysical evidence for separate channels for the perception of form, color, movement, and
depth. J. Neurosci. 7, 3416–3468 (1987).
5. Komatsu, H., Kinoshita, M. & Murakami, I. Neural responses in the retinotopic representation of the blind spot in the macaque
V1 to stimuli for perceptual filling-in. J. Neurosci. 20, 9310–9319 (2000).
6. Spillmann, L. From perceptive fields to Gestalt. Prog. Brain Res. 155, 67–92 (2006).
7. Martinez-Conde, S., Macknik, S. L., Troncoso, X. G. & Dyar, T. A. Microsaccades counteract visual fading during fixation. Neuron
49, 297–305. https://doi.org/10.1016/j.neuron.2005.11.033 (2006).
8. McCamy, M. B. et al. Microsaccadic efficacy and contribution to foveal and peripheral vision. J. Neurosci. 32, 9194–9204. https://
doi.org/10.1523/JNEUROSCI.0515-12.2012 (2012).
9. McCamy, M. B., Macknik, S. L. & Martinez-Conde, S. Different fixational eye movements mediate the prevention and the reversal
of visual fading. J. Physiol. 592, 4381–4394. https://doi.org/10.1113/jphysiol.2014.279059 (2014).
10. Costela, F. M., McCamy, M. B., Macknik, S. L., Otero-Millan, J. & Martinez-Conde, S. Microsaccades restore the visibility of minute
foveal targets. PeerJ 1, e119. https://doi.org/10.7717/peerj.119 (2013).
11. Costela, F. M. et al. Changes in visibility as a function of spatial frequency and microsaccade occurrence. Eur. J. Neurosci. 45,
433–439 (2017).
12. Troncoso, X. G., Macknik, S. L. & Martinez-Conde, S. Microsaccades counteract perceptual filling-in. J. Vis. 8(15), 11–19. https
://doi.org/10.1167/8.14.15 (2008).
13. Alexander, R. G. & Martinez-Conde, S. in Eye Movement Research Studies in Neuroscience, Psychology and Behavioral Economics:
An introduction to the scientific foundations of eye movement research and its applications. (eds Cristoph Klein & Ulrich Ettinger)
73–115 (Springer, Cham, 2019).
14. Engbert, R. & Kliegl, R. Microsaccades uncover the orientation of covert attention. Vision. Res. 43, 1035–1045 (2003).
15. Engbert, R. & Mergenthaler, K. Microsaccades are triggered by low retinal image slip. Proc. Natl. Acad. Sci. U S A 103, 7192–7197.
https://doi.org/10.1073/pnas.0509557103 (2006).
16. Laubrock, J., Engbert, R. & Kliegl, R. Microsaccade dynamics during covert attention. Vis. Res. 45, 721–730. https://doi.
org/10.1016/j.visres.2004.09.029 (2005).
17. Engbert, R. Microsaccades: A microcosm for research on oculomotor control, attention, and visual perception. Prog. Brain Res.
154, 177–192 (2006).
18. Rolfs, M., Laubrock, J. & Kliegl, R. Shortening and prolongation of saccade latencies following microsaccades. Exp. Brain Res. 169,
369–376. https://doi.org/10.1007/s00221-005-0148-1 (2006).
19. Moller, F., Laursen, M. L., Tygesen, J. & Sjolie, A. K. Binocular quantification and characterization of microsaccades. Graefes Arch.
Clin. Exp. Ophthalmol. 240, 765–770. https://doi.org/10.1007/s00417-002-0519-2 (2002).
20. Spillmann, L. & Kurtenbach, A. Dynamic noise backgrounds facilitate target fading. Vis. Res. 32, 1941–1946 (1992).
21. van Dam, L. C. & van Ee, R. The role of (micro)saccades and blinks in perceptual bi-stability from slant rivalry. Vis. Res. 45,
2417–2435. https://doi.org/10.1016/j.visres.2005.03.013 (2005).
22. van Dam, L. C. & van Ee, R. Retinal image shifts, but not eye movements per se, cause alternations in awareness during binocular
rivalry. J. Vis. 6, 1172–1179 (2006).
23. 23van Dam, L. C. & van Ee, R. The role of saccades in exerting voluntary control in perceptual and binocular rivalry. Vision research
46, 787–799, doi:https://doi.org/10.1016/j.visres.2005.10.011 (2006).
24. Clarke, F. J. J. & Belcher, S. J. On the localization of Troxler’s effect in the visual pathway. Vis. Res. 2, 53–68. https://doi.
org/10.1016/0042-6989(62)90063-9 (1962).
25. Krauskopf, J. Effect of retinal image stabilization on the appearance of heterochromatic targets. J. Opt. Soc. Am. 53, 741–744 (1963).
26. Komatsu, H., Murakami, I. & Kinoshita, M. Surface representation in the visual system. Cogn. Brain Res. 5, 97–104 (1996).
27. Otero-Millan, J., Macknik, S. L. & Martinez-Conde, S. Microsaccades and blinks trigger illusory rotation in the “rotating snakes”
illusion. J. Neurosci. 32, 6043. https://doi.org/10.1523/JNEUROSCI.5823-11.2012 (2012).
28. Rollins, M. What Monet meant: Intention and attention in understanding art. J. Aesthet. Art Crit. 62, 175–188 (2004).
Acknowledgements
This work was supported by the National Science Foundation (Award 1734887 to SMC and SLM), the National
Eye Institute (Award R01-EY031971 to SMC and SLM), the Empire Innovation Program (Awards to SMC and
SLM) and a fellowship from “la Caixa” Foundation (ID 100010434) awarded to JC (fellowship code LCF/BQ/
AA17/11610017). We thank Jorge Otero-Millan for his advice on microsaccade direction analyses.
Author contributions
R.G.A., S.L.M., and S.M.C. conceptualized, planned, and supervised the project. R.G.A. and S.M.C. wrote the
main manuscript text. J.C. and R.G.A. collected the data. A.V. and R.G.A. conducted formal analyses of the data,
and A.V., J.C., and R.G.A. prepared the figures and tables. All authors reviewed the manuscript.
Competing interests
The authors declare no competing interests.
Additional information
Supplementary Information The online version contains supplementary material available at https://doi.
org/10.1038/s41598-021-82222-3.
Correspondence and requests for materials should be addressed to S.M.-C.
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